diff --git a/src/Servers/Kestrel/Core/src/Internal/Http/HttpRequestHeaders.cs b/src/Servers/Kestrel/Core/src/Internal/Http/HttpRequestHeaders.cs
index cdd6ecac601d..3fbcc4854f42 100644
--- a/src/Servers/Kestrel/Core/src/Internal/Http/HttpRequestHeaders.cs
+++ b/src/Servers/Kestrel/Core/src/Internal/Http/HttpRequestHeaders.cs
@@ -98,7 +98,13 @@ private void AppendContentLength(ReadOnlySpan<byte> value)
             KestrelBadHttpRequestException.Throw(RequestRejectionReason.MultipleContentLengths);
         }
 
-        if (!Utf8Parser.TryParse(value, out long parsed, out var consumed) ||
+        // Per RFC 9110 §8.6, Content-Length is 1*DIGIT: only ASCII digits are allowed.
+        // https://www.rfc-editor.org/rfc/rfc9110.html#section-8.6
+        // Utf8Parser.TryParse accepts a leading '+' or '-' sign, so ensure the first byte is a digit.
+        long parsed = 0;
+        if (value.IsEmpty ||
+            value[0] is < (byte)'0' or > (byte)'9' ||
+            !Utf8Parser.TryParse(value, out parsed, out var consumed) ||
             parsed < 0 ||
             consumed != value.Length)
         {
@@ -122,8 +128,11 @@ private unsafe void AppendContentLengthCustomEncoding(ReadOnlySpan<byte> value,
         var numChars = customEncoding.GetChars(value, decodedChars);
         long parsed = -1;
 
+        // Per RFC 9110 §8.6, Content-Length is 1*DIGIT. NumberStyles.None
+        // https://www.rfc-editor.org/rfc/rfc9110.html#section-8.6
+        // disallows leading signs and whitespace that NumberStyles.Integer would accept.
         if (numChars > 19 ||
-            !long.TryParse(decodedChars.Slice(0, numChars), NumberStyles.Integer, CultureInfo.InvariantCulture, out parsed) ||
+            !long.TryParse(decodedChars.Slice(0, numChars), NumberStyles.None, CultureInfo.InvariantCulture, out parsed) ||
             parsed < 0)
         {
             KestrelBadHttpRequestException.Throw(RequestRejectionReason.InvalidContentLength, value.GetRequestHeaderString(HeaderNames.ContentLength, EncodingSelector, checkForNewlineChars: false));
diff --git a/src/Servers/Kestrel/Core/test/HttpRequestHeadersTests.cs b/src/Servers/Kestrel/Core/test/HttpRequestHeadersTests.cs
index 7a9b6dea0f78..66aca720f271 100644
--- a/src/Servers/Kestrel/Core/test/HttpRequestHeadersTests.cs
+++ b/src/Servers/Kestrel/Core/test/HttpRequestHeadersTests.cs
@@ -710,6 +710,27 @@ public void CanSpecifyEncodingForContentLength()
             new HttpRequestHeaders().Append(contentLengthNameBytes, contentLengthValueBytes, checkForNewlineChars: false));
     }
 
+    [Theory]
+    [InlineData("+1")]
+    [InlineData("+0")]
+    [InlineData("-0")]
+    [InlineData("-1")]
+    [InlineData(" 1")]
+    [InlineData("1a")]
+    [InlineData("")]
+    public void ContentLengthWithCustomEncodingRejectsNonDigits(string value)
+    {
+        var contentLengthNameBytes = Encoding.ASCII.GetBytes(HeaderNames.ContentLength);
+        var contentLengthValueBytes = Encoding.UTF32.GetBytes(value);
+
+        var headers = new HttpRequestHeaders(encodingSelector: _ => Encoding.UTF32);
+
+#pragma warning disable CS0618 // Type or member is obsolete
+        Assert.Throws<BadHttpRequestException>(() =>
+#pragma warning restore CS0618 // Type or member is obsolete
+            headers.Append(contentLengthNameBytes, contentLengthValueBytes, checkForNewlineChars: false));
+    }
+
     [Fact]
     public void ValueReuseNeverWhenUnknownHeader()
     {
diff --git a/src/Servers/Kestrel/test/InMemory.FunctionalTests/BadHttpRequestTests.cs b/src/Servers/Kestrel/test/InMemory.FunctionalTests/BadHttpRequestTests.cs
index 05481529b5ea..cb49b2822307 100644
--- a/src/Servers/Kestrel/test/InMemory.FunctionalTests/BadHttpRequestTests.cs
+++ b/src/Servers/Kestrel/test/InMemory.FunctionalTests/BadHttpRequestTests.cs
@@ -100,6 +100,10 @@ public Task BadRequestIfMethodRequiresLengthButNoContentLengthInHttp10Request(st
     [Theory]
     [InlineData("NaN")]
     [InlineData("-1")]
+    [InlineData("+1")]
+    [InlineData("+0")]
+    [InlineData("-0")]
+    [InlineData("")]
     public Task BadRequestIfContentLengthInvalid(string contentLength)
     {
         return TestBadRequest(